On the mechanism of respiratory complex I

Journal of Bioenergetics and Biomembranes

Volumn 46, Issue 4, 2014, Pages 255-268

  Friedrich, Thorsten ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

(ubi) quinone; Electron transfer; Energy coupling; Iron sulfur clusters; NADH:ubiquinone oxidoreductase; Proton translocation

Indexed keywords

AROMATIC AMINO ACID; IRON; QUINONE DERIVATIVE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SULFUR; UBIQUINONE; FLAVINE MONONUCLEOTIDE; LIPID BILAYER; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTON;

BINDING AFFINITY; ELECTRON TRANSPORT; ENZYME BINDING; ENZYME SUBSTRATE COMPLEX; MITOCHONDRIAL RESPIRATION; MOLECULAR DYNAMICS; MUTAGENESIS; NOMENCLATURE; NONHUMAN; NUCLEOTIDE BINDING SITE; PROTON TRANSPORT; SHORT SURVEY; BINDING SITE; CHEMISTRY; ION TRANSPORT; LIPID BILAYER; METABOLISM; PHYSIOLOGY;

BINDING SITES; ELECTRON TRANSPORT COMPLEX I; FLAVIN MONONUCLEOTIDE; ION TRANSPORT; LIPID BILAYERS; NAD; PROTONS; UBIQUINONE;

EID: 84906314649     PISSN: 0145479X     EISSN: 15736881     Source Type: Journal    
DOI: 10.1007/s10863-014-9566-8     Document Type: Short Survey

References (114)

1. Amarneh B, Vik SB (2003) Mutagenesis of subunit N of the Escherichia coli complex I identification of the initiation codon and the sensitivity of mutants to decylubiquinone. Biochemistry 42:4800-4808 (Pubitemid 36532031)
2. Angerer H, Nasiri HR, NiedergesäßV, Kerscher S, Schwalbe H, Brandt U (2012) Tracing the tail of ubiquinone in mitochondrial complex I. Biochim Biophys Acta 1817:1776-1784
3. Auriol C, Bestel-Corre G, Claude JB, Soucaille P, Meynial-Salles I (2011) Stress-induced evolution of Escherichia coli points to original concepts in respiratory cofactor selectivity. Proc Natl Acad Sci U S A 108:1278-1283
4. Baradaran R, Berrisford JM, Minhas GS, Sazanov LA (2013) Crystal structure of the entire respiratory complex I. Nature 494:443-448
5. Baranova EA, Holt PJ, Sazanov LA (2007) Single particle analysis confirms distal location of subunits NuoL and NuoM in Escherichia coli complex I. J Mol Biol 366:140-154
6. Belevich G, Euro L, Wikström M, Verkhovskaya M (2007) Role of the conserved arginine 274 and histidine 224 and 228 residues in the NuoCD subunit of complex I from Escherichia coli. Biochemistry 46:526-533 (Pubitemid 46105441)
7. Belevich G, Knuuti J, Verkhovsky MI, Wikström M, Verkhovskaya M (2011) Probing the mechanistic role of the long α-helix in subunit L of respiratory complex I from Escherichia coli by site-directed mutagenesis. Mol Microbiol 82:1086-1095
8. Berrisford JM, Sazanov LA (2009) Structural basis for the mechanism of respiratory complex I. J Biol Chem 284:29773-29783
9. Birrell JA, Hirst J (2010) Truncation of subunit ND2 disrupts the three-fold symmetry of the antiporter-like subunits in complex I from higher metazoans. FEBS Lett 584:4247-4252
10. Birrell JA, Morina K, Bridges HR, Friedrich T, Hirst J (2013) Investigating the function of [2Fe-2S] cluster N1a, the off-pathway cluster in complex I, by manipulating its reduction potential. Biochem J 456:139-146
11. - stoichiometry for NADH dehydrogenase I and dimethyl sulfoxide reductase in anaerobically grown Escherichia coli cells. J Bacteriol 178:6233-6237
12. Brandt U (2006) Energy converting NADH:quinone oxidoreductase (complex I). Annu Rev Biochem 75:69-92
13. Clason T, Ruiz T, Schägger H, Peng G, Zickermann V, Brandt U, Michel H, Radermacher M (2010) The structure of eukaryotic and prokaryotic complex I. J Struct Biol 169:81-88
14. Darrouzet E, Issartel JP, Lunardi J, Dupuis A (1998) The 49-kDa subunit of NADH-ubiquinone oxidoreductase (Complex I) is involved in the binding of piericidin and rotenone, two quinone-related inhibitors. FEBS Lett 431:34-38 (Pubitemid 28330847)
15. Djavadi-Ohaniance L, Hatefi Y (1975) Oxidation of NADPH by submitochondrial particles from beef heart in complete absence of transhydrogenase activity from NADPH to NAD. J Biol Chem 250:9397-9403
16. Efremov RG, Baradaran R, Sazanov LA (2010) The architecture of respiratory complex I. Nature 465:441-445
17. Ernster L, Hoberman HD, Howard RL, King TE, Lee CP, Mackler B, Sottocasa G (1965) Stereospecificity of certain soluble and particulate preparations of mitochondrial reduced nicotinamide-adenine dinucleotide dehydrogenase from beef heart. Nature 207:940-941
18. Fearnley IM, Walker JE (1992) Conservation of sequences of subunits of mitochondrial complex I and their relationships with other proteins. Biochim Biophys Acta 1140:105-134
19. Fisher N, Rich PR (2000) A motif for quinone binding sites in respiratory and photosynthetic systems. J Mol Biol 296:1153-1162
20. Friedrich T (1998) The NADH: Ubiquinone oxidoreductase (complex I) from Escherichia coli. Biochim Biophys Acta 1364:134-146
21. Friedrich T (2001) Complex I: A chimaera of a redox and conformation driven proton-pump? J Bioenerg Biomembr 33:169-179
22. Friedrich T, Hellwig P (2010) Redox-induced conformational changes within the Escherichia coli NADH ubiquinone oxidoreductase (complex I): an analysis by mutagenesis and FTIR spectroscopy. Biochim Biophys Acta 1797:659-663
23. Friedrich T, Scheide D (2000) The respiratory complex I of bacteria, archaea and eukarya and itsmodule commonwithmembrane-bound multisubunit hydrogenases. FEBS Lett 479:1-5 (Pubitemid 30625247)
24. Friedrich T, Weiss H (1997) Modular evolution of the respiratory NADH: ubiquinone oxidoreductase and the origin of its modules. J Theor Biol 187:529-541
25. Friedrich T, Steinmüller K, Weiss H (1995) The proton-pumping respiratory complex I of bacteria and mitochondria and its homologue in chloroplasts. FEBS Lett 367:107-111
26. Galkin A, Brandt U (2005) Superoxide radical formation by pure complex I (NADH:ubiquinone oxidoreductase) from Yarrowia lipolytica. J Biol Chem 280:30129-30135 (Pubitemid 41216190)
27. Galkin A, Dröse S, Brandt U (2006) The proton pumping stoichiometry of purified mitochondrial complex I reconstituted in proteoliposomes. Biochim Biophys Acta 1757:1575-1581 (Pubitemid 44841960)
28. Golinelli MP, Akin LA, Crouse BR, Johnson MK, Meyer J (1996) Cysteine lignad swapping on a deletable loop of the [2Fe-2S] ferredoxin from Clostridium pasteurianum. Biochemistry 35:8995-9002 (Pubitemid 26242321)
29. Golinelli MP, Chatelet C, Duin EC, Johnson MK, Meyer J (1998) Extensive ligand rearrangements around the [2Fe-2S] cluster of Clostridium pasteurianum ferredoxin. Biochemistry 37:10429-10437 (Pubitemid 28357565)
30. Gong X, Xie T, Yu L, Hesterberg M, Scheide D, Friedrich T, Yu CA (2003) The ubiquinone-binding site in NADH:ubiquinone oxidoreductase from Escherichia coli. J Biol Chem 278:25731-25737 (Pubitemid 36835329)
31. Grigorieff N (1999) Structure of the respiratory NADH:ubiquinone oxidoreductase (complex I). Curr Opin Struct Biol 9:476-483
32. Guénebaut V, Schlitt A, Weiss H, Leonard K, Friedrich T (1998) Consistent structure between bacterial and mitochondrial NADH: ubiquinone oxidoreductase (Complex I). J Mol Biol 276:105-112 (Pubitemid 28085412)
33. Gunner MR, Saleh MA, Cross E, ud-Doula A, Wise M (2000) Backbone diploes generate positive potentials in all proteins: origins and implications of the effect. Biophys J 78:1126-1144 (Pubitemid 30141542)
34. Gurrath M, Friedrich T (2004) Adjacent cysteines are capable of ligating the same tetranuclear iron-sulfur cluster. Proteins Struct Funct Bioinforma 56:556-563 (Pubitemid 38924967)
35. Hatefi Y, Hanstein WG (1973) Interactions of reduced and oxidized triphosphopyridine nucleotides with the electron-transport system of bovine heart mitochondria. Biochemistry 12:3515-3522
36. Hayashi T, Stuchebrukhov AA (2010) Electron tunneling in respiratory complex I. Proc Natl Acad Sci U S A 107:19157-19162
37. Hellwig P, Scheide D, Bungert S, Mäntele W, Friedrich T (2000) FTIR spectroscopic characterization of NADH:ubiquinone oxidoreductase (complex I) from Escherichia coli: oxidation of FeS cluster N2 is coupled with the protonation of an aspartate or glutamate side chain. Biochemistry 39:10884-10891
38. Hielscher R, Yegres M, Voicescu M, Gnandt E, Friedrich T, Hellwig P (2013) Characterization of two quinone radicals in the NADH: ubiquinone oxidoreductase from Escherichia coli by a combined fluorescence spectroscopic and electrochemical approach. Biochemistry 52:8993-9000
39. Hinchliffe P, Carroll J, Sazanov LA (2006) Identification of a novel subunit of respiratory complex I from Thermus thermophilus. Biochemistry 45:4413-4420
40. Hirst J (2013) Mitochondrial complex I. Annu Rev Biochem 82:551-575
41. Hubbell WL, Mchaourab HS, Altenbach C, Lietzow MA (1996) Watching proteins move using site-directed spin labelling. Structure 4:779-783 (Pubitemid 26312362)
42. Hunte C, Zickermann V, Brandt U (2010) Functional modules and structural basis of conformational coupling in mitochondrial complex I. Science 329:448-451
43. Ifuku K, Endo T, Shikanai T, Aro EM (2011) Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant Cell Physiol 52:1560-1568
44. Ingledew WJ, Ohnishi T (1980) An analysis of some thermodynamic properties of iron-sulphur centres in site I of mitochondria. Biochem J 186:111-117
45. Jeschke G (2002) Distance measurements in the nanometer range by pulse EPR. Chem Phys Chem 3:927-932
46. Kaila VR, Wikström M, Hummer G (2014) Electrostatics, hydration, and proton transfer dynamics in the membrane domain of respiratory complex I. Proc Natl Acad Sci U S A 111:6988-6993
47. Kashani-Poor N, Zwicker K, Kerscher S, Brandt U (2001) A central functional role for the 49-kDa subunit within the catalytic core of mitochondrial complex I. J Biol Chem 276:24082-24087
48. Kikuno R, Miyata T (1985) Sequence homologies among mitochondrial DNA-coded URF2, URF4 and URF5. FEBS Lett 189:85-88 (Pubitemid 15227712)
49. Knuuti J, Belevich G, Sharma V, Bloch DA, Verkhovskaya M (2013) A single amino acid residue controls ROS production in the respiratory Complex I from Escherichia coli. Mol Microbiol 90:1190-1200
50. Kohlstädt M, Dörner K, Labatzke R, Koç C, Hielscher R, Schiltz E, Einsle O, Hellwig P, Friedrich T (2008) Heterologous production, isolation, characterization and crystallization of a soluble fragment of the NADH:ubiquinone oxidoreductase (complex I) from Aquifex aeolicus. Biochemistry 47:13036-13045
51. Kussmaul L, Hirst J (2006) The mechanism of superoxide production by NADH:ubiquinone oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci U S A 103:7607-7612
52. Lesk AM (1995) NAD-binding domains of dehydrogenases. Curr Opin Struct Biol 5:775-783
53. Masuya T, Murai M, Ifuku K, Morisaka H, Miyoshi H (2014) Site-specific chemical labeling of mitochondrial respiratory complex I through ligand-directed tosylate chemistry. Biochemistry 53:2307-2317
54. Mathiesen C, Hagerhall C (2003) The 'antiporter module' of respiratory chain complex I includes the MrpC/NuoK subunit - a revision of the modular evolution scheme. FEBS Lett 549:7-13 (Pubitemid 36959834)
55. Meyer J, Andrade SL, Einsle O (2008) Thioredoxin-like [2Fe-2S] ferredoxin, Handbook of Metalloproteins (Messerschmidt, A., ed.) John Wiley & Sons, New York
56. Moparthi VK, Kumar B, Mathiesen C, Hägerhäll C (2011) Homologous protein subunits from Escherichia coli NADH:quinone oxidoreductase can functionally replace MrpA and MrpD in Bacillus subtilis. Biochim Biophys Acta 1807:427-436
57. Morina K, Schulte M, Hubrich F, Dörner K, Steimle S, Stolpe S, Friedrich T (2011) Engineering the respiratory complex I to an energy-converting NADPH:ubiquinone oxidoreductase. J Biol Chem 286:34627-34634
58. Moser CC, Farid TA, Chobot SE, Dutton PL (2006) Electron tunneling chains of mitochondria. Biochim Biophys Acta 1757:1096-1109 (Pubitemid 44472548)
59. Nakamaru-Ogiso E, Sakamoto K, Matsuno-Yagi A, Miyoshi H, Yagi T (2003) The ND5 subunit was labeled by a photoaffinity analogue of fenpyroximate in bovinemitochondrial complex I. Biochemistry 42:746-754 (Pubitemid 36133299)
60. Nakamaru-Ogiso E, Yano T, Yagi T, Ohnishi T (2005) Characterization of the iron-sulfur cluster N7 (N1c) in the subunit NuoG of the proton-translocating NADH-quinone oxidoreductase from Escherichia coli. J Biol Chem 280:301-307 (Pubitemid 40164993)
61. Nakamaru-Ogiso E, Han H, Matsuno-Yagi A, Keinan E, Sinha SC, Yagi T, Ohnishi T (2010) The ND2 subunit is labeled by a photoaffinity analogue of asimicin, a potent complex I inhibitor. FEBS Lett 584:883-888
62. Ohnishi T (1998) Iron-sulfur clusters/semiquinones in complex I. Biochim Biophys Acta 1364:186-206
63. Ohnishi T (2010) Piston drives a proton pump. Nature 465:428-429
64. Ohnishi T, Nakamaru-Ogiso E (2008) Were there any " misassignments" among iron-sulfur clusters N4, N5 and N6b in NADH-quinone oxidoreductase (complex I)? Biochim Biophys Acta 1777:703-710
65. Ohnishi T, Salerno JC (2005) Conformation-driven and semiquinonegated proton-pump mechanism in the NADH-ubiquinone oxidoreductase (complex I). FEBS Lett 579:4555-4561 (Pubitemid 41218626)
66. Ohnishi ST, Salerno JC, Ohnishi T (2010a) Possible roles of two quinone molecules in direct and indirect proton pumps of bovine heart NADH-quinone oxidoreductase (complex I). Biochim Biophys Acta 1797:1891-1893
67. Ohnishi T, Nakamaru-Ogiso E, Ohnishi ST (2010b) A new hypothesis on the simultaneous direct and indirect proton pump mechanisms in NADH-quinone oxidoreductase (complex I). FEBS Lett 584:4131-4137
68. Ohnishi ST, Shinzawa-Itoh K, Ohta K, Yoshikawa S, Ohnishi T (2010c) New insights into the superoxide generation sites in bovine heart NADH-ubiquinone oxidoreductase (Complex I): the significance of protein-associated ubiquinone and the dynamic shifting of generation sites between semiflavin and semiquinone radicals. Biochim Biophys Acta 1797:1901-1909
69. Ohshima M, Miyoshi H, Sakamoto K, Takegami K, Iwata J, Kuwabara K, Iwamura H, Yagi T (1998) Characterization of the ubiquinone reduction site of mitochondrial complex I using bulky synthetic ubiquinones. Biochemistry 37:6436-6445 (Pubitemid 28213664)
70. Peng G, Fritzsch G, Zickermann V, Schägger H, Mentele R, Lottspeich F, Bostina M, Radermacher M, Huber R, Stetter KO, Michel H (2003) Isolation, characterization and electron microscopic single particle analysis of the NADH:ubiquinone oxidoreductase (complex I) from the hyperthermophilic eubacterium Aquifex aeolicus. Biochemistry 42:3032-3039 (Pubitemid 36331547)
71. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853-1858 (Pubitemid 28555258)
72. Pohl T, Uhlmann M, Kaufenstein M, Friedrich T (2007a) Lambda Redmediated mutagenesis and efficient large scale affinity purification of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I). Biochemistry 46:10694-10702 (Pubitemid 47417261)
73. Pohl T, Bauer T, Dörner K, Stolpe S, Sell P, Zocher G, Friedrich T (2007b) Iron-sulfur cluster N7 of the NADH:ubiquinone oxidoreductase (complex I) is essential for stability but not involved in electron transfer. Biochemistry 46:6588-6596 (Pubitemid 46870124)
74. Pohl T, Walter J, Stolpe S, Defeu Soufo HJ, Graumann PL, Friedrich T (2007c) Effects of the deletion of the Escherichia coli frataxin homologue CyaY on the respiratory NADH:ubiquinone oxidoreductase. BMC Biochem 8:13
75. Pohl T, Spatzal T, Aksoyoglu M, Schleicher E, Rostas AM, Lay H, Glessner U, Boudon C, Hellwig P, Weber S, Friedrich T (2010) Spin labeling of the Escherichia coli NADH:ubiquinone oxidoreductase (complex I). Biochim Biophys Acta 1797:1894-1900
76. Roessler MM, King MS, Robinson AJ, Armstrong FA, Harmer J, Hirst J (2010) Direct assignment of EPR spectra to structurally defined iron-sulfur clusters in complex I by double electron - electron resonance. Proc Natl Acad Sci U S A 107:1930-1935
77. Rothery RA, Workun GJ, Weiner JH (2008) The prokaryotic complex iron-sulfur molybdoenzyme family. Biochim Biophys Acta 1778:1897-1929
78. Sato M, Sinha PK, Torres-Bacete J, Matsuno-Yagi A, Yagi T (2013) Energy transducing roles of antiporter-like subunits in Escherichia coli NDH-1 with main focus on subunit NuoN (ND2). J Biol Chem 288:24705-24716
79. Sazanov LA, Hinchliffe P (2006) Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311:1430-1436 (Pubitemid 43376691)
80. Sazanov LA, Baradaran R, Efremov RG, Berrisford JM, Minhas G (2013) A long road towards the structure of respiratory complex I, a giant molecular proton pump. Biochem Soc Trans 41:1265-1271
81. Schuler F, Yano T, DiBernardo S, Yagi T, Yankovskaya V, Singer T, Casida JE (1999) NADH-quinone oxidoreductase: PSST subunit couples electron transfer from iron-sulfur cluster N2 to quinone. Proc Natl Acad Sci U S A 96:4149-4153 (Pubitemid 29169051)
82. Screpanti E, Hunte C (2007) Discontinuous membrane helices in transport proteins and their correlation with function. J Struct Biol 159:261-267 (Pubitemid 47095395)
83. Sekiguchi K, Murai M, Miyoshi H (2009) Exploring the binding site of acetogenin in the ND1 subunit of bovine mitochondrial complex I. Biochim Biophys Acta 1787:1106-1111
84. Sharpley MS, Shannon RJ, Draghi F, Hirst J (2006) Interactions between phospholipids and NADH:ubiquinone oxidoreductase (complex I) from bovine mitochondria. Biochemistry 45:241-248 (Pubitemid 43054102)
85. Sled VD, Rudnitzky NI, Hatefi Y, Ohnishi T (1994) Thermodynamic analysis of flavin in mitochondrial NADH:ubiquinone oxidoreductase (complex I). Biochemistry 33:10069-10075 (Pubitemid 24286086)
86. Steimle S, Bajzath C, Dörner K, Schulte M, Bothe V, Friedrich T (2011) Role of subunit NuoL for proton translocation by respiratory complex I. Biochemistry 50:3386-3393
87. Steimle S, Willistein M, Hegger P, Janoschke M, Erhardt H, Friedrich T (2012) Asp563 of the horizontal helix of subunit NuoL is involved in proton translocation by the respiratory complex I. FEBS Lett 586:699-704
88. Steinhoff HJ, Radzwill N, Thevis W, Lenz V, Brandenburg D, Antson A, Dodson G, Wollmer A (1997) Determination of interspin distances between spin labels attached to insulin: comparison of electron paramagnetic resonance data with the X-ray structure. Biophys J 73:3287-3298 (Pubitemid 27525791)
89. Stolpe S, Friedrich T (2004) The Escherichia coli NADH:ubiquinone oxidoreductase (complex I) is a primary proton pump but may be capable of secondary sodium antiport. J Biol Chem 279:18377-18383 (Pubitemid 38623253)
90. Tocilescu MA, Zickermann V, Zwicker K, Brandt U (2010) Quinone binding and reduction by respiratory complex I. Biochim Biophys Acta 1797:1883-1890
91. Torres-Bacete J, Sinha PK, Matsuno-Yagi A, Yagi T (2011) Structural contribution of C-terminal segments of NuoL (ND5) and NuoM (ND4) subunits of complex I from Escherichia coli. J Biol Chem 286:34007-34014
92. Unden G, Bongaerts J (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217-234 (Pubitemid 27283364)
93. van Hellemond JJ, van der Klei A, van Weelden SW, Tielens AG (2003) Biochemical and evolutionary aspects of anaerobically functioning mitochondria. Philos Trans R Soc Lond B Biol Sci 358:205-213
94. Verkhovskaya M, Wikström M (2014) Oxidoreduction properties of bound ubiquinone in complex I from Escherichia coli. Biochim Biophys Acta 1837:246-250
95. Verkhovskaya ML, Belevich N, Euro L, Wikström M, Verkhovsky MI (2008) Real-time electron transfer in respiratory complex I. Proc Natl Acad Sci U S A 105:3763-3767 (Pubitemid 351723472)
96. Vinogradov AD (1998) Catalytic properties of the mitochondrial NADH-ubiquinone oxidoreductase (complex I) and the pseudo-reversible active/inactive enzyme transition. Biochim Biophys Acta 1364:169-185
97. Walker JE (1992) The NADH:ubiquinone oxidoreductase (complex I) of respiratory chains. Q Rev Biophys 25:253-324
98. Weidner U, Geier S, Ptock A, Friedrich T, Leif H, Weiss H (1993) The gene locus of the proton-translocating NADH: ubiquinone oxidoreductase in Escherichia coli. JMol Biol 233:109-122
99. Weiss H, Friedrich T, Hofhaus G, Preis D (1991) The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur J Biochem 197:563-576
100. Wikström M (1984) Two protons are pumped from the mitochondrial matrix per electron transferred between NADH and ubiquinone. FEBS Lett 169:300-304
101. Wikström M, Hummer G (2012) Stoichiometry of proton translocation by respiratory complex I and its mechanistic implications. Proc Natl Acad Sci U S A 109:4431-4436
102. Williams TA, Foster PG, Cox CJ, Embley TM (2013) An archaeal origin of eukaryotes supports only two primary domains of life. Nature 504:231-236
103. Wittekindt C, Schwarz M, Friedrich T, Koslowski T (2009) Aromatic amino acids as stepping stones in charge transfer in respiratory complex I: an unusual mechanism deduced from atomistic theory and bioinformatics. J Am Chem Soc 131:8134-8140
104. Yagi T (1986) Purification and characterization of NADH dehydrogenase complex from Paracoccus denitrificans. Arch Biochem Biophys 250:302-311
105. Yagi T, Matsuno-Yagi A (2003) The proton-translocating NADH-quinone oxidoreductase in the respiratory chain: the secret unlocked. Biochemistry 42:2266-2274 (Pubitemid 36255200)
106. Yagi T, Yano T, Matsuno-Yagi A (1993) Characteristics of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans as revealed by biochemical, biophysical, and molecular biological approaches. J Bioenerg Biomembr 25:339-345
107. Yagi T, Yano T, DiBernardo S, Matsuno-Yagi A (1998) Procaryotic complex I (NDH-1), an overview. Biochim Biophys Acta 1364:125-133
108. Yano T, Chu SS, Sled, VD, Ohnishi, T, Yagi, T (1997) The proton-translocating NADH-quinone oxidoreductase (NDH-1) of the thermophilic bacterium Thermus thermophilus HB-8. J Biol Chem 272:4201-4211
109. Yano T, Magnitsky S, Ohnishi T (2000) Characterization of the complex I-associated ubisemiquinone species: toward the understanding of their functional roles in the electron/proton transfer reaction. Biochim Biophys Acta 1459:299-304 (Pubitemid 30612400)
110. Nf) and the interaction with cluster N2: new insight into the energy-coupled electron transfer in complex I. Biochemistry 44:1744-1754
111. Yeh AP, Ambroggio XI, Andrade SLA, Einsle O, Chatelet C, Meyer J, Rees DC (2002) High resolution crystal structures of the wild type and Cys-55 → Ser and Cys-59 → Ser variants of the thioredoxinlike [2Fe-2S] ferredoxin from Aquifex aeolicus. J Biol Chem 277:34499-34507
112. Yip CY, Harbour ME, Jayawardena K, Fearnley IM, Sazanov LA (2011) Evolution of respiratory complex I: "supernumerary" subunits are present in the alpha-proteobacterial enzyme. J Biol Chem 286:5023-5033
113. Zickermann V, Bostina M, Hunte C, Ruiz T, Radermacher M, Brandt U (2003) Functional implications from an unexpected position of the 49-kDa subunit of NADH:ubiquinone oxidoreductase. J Biol Chem 278:29072-29078 (Pubitemid 36935821)
114. Zwicker K, Galkin A, Dröse S, Grgic L, Kerscher S, Brandt U (2006) The redox-bohr group associated with iron-sulfur cluster N2 of complex I. J Biol Chem 281:23013-23017